De novo transcriptome sequencing of axolotl blastema for identification of differentially expressed genes during limb regeneration

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Wu, Cheng Han ^a   Tsai, Mong Hsun ^a,c   Ho, Chia Chuan ^a   Chen, Chien Yu ^a   Lee, Hsuan Shu ^a,b,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

Author keywords

Ambystoma mexicanum; Axolotl; Blastema; De novo transcriptome sequencing; Transcriptome

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTOME; COMPLEMENTARY DNA; SIGNAL PEPTIDE;

AMBYSTOMA; ARTICLE; BLASTEMA; CONTROLLED STUDY; DNA SEQUENCE; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; IN SITU HYBRIDIZATION; LIMB REGENERATION; METABOLISM; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; AMBYSTOMA MEXICANUM; AMPUTATION; ANIMAL; CLUSTER ANALYSIS; DENERVATION; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; INNERVATION; LIMB; MOLECULAR GENETICS; PHYSIOLOGY; REGENERATION; REPRODUCIBILITY; SEQUENCE HOMOLOGY; SURGERY; TIME;

AMBYSTOMA MEXICANUM; SALAMANDROIDEA; VERTEBRATA;

AMBYSTOMA MEXICANUM; AMPUTATION; ANIMALS; CLUSTER ANALYSIS; DENERVATION; DNA, COMPLEMENTARY; EXTREMITIES; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE ANNOTATION; REGENERATION; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84879488712     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-434     Document Type: Article

References (53)

1. Brockes JP. Amphibian limb regeneration: rebuilding a complex structure. Science 1997, 276:81-87. 10.1126/science.276.5309.81, 9082990.
2. Satoh A, Graham GM, Bryant SV, Gardiner DM. Neurotrophic regulation of epidermal dedifferentiation during wound healing and limb regeneration in the axolotl (Ambystoma mexicanum). Dev Biol 2008, 319:321-335. 10.1016/j.ydbio.2008.04.030, 18533144.
3. Ferris DR, Satoh A, Mandefro B, Cummings GM, Gardiner DM, Rugg EL. Ex vivo generation of a functional and regenerative wound epithelium from axolotl (Ambystoma mexicanum) skin. Dev Growth Differ 2010, 52:715-724. 10.1111/j.1440-169X.2010.01208.x, 20874715.
4. Yang EV, Gardiner DM, Carlson MR, Nugas CA, Bryant SV. Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev Dyn 1999, 216:2-9. 10.1002/(SICI)1097-0177(199909)216:1<2::AID-DVDY2>3.0.CO;2-P, 10474160.
5. Satoh A, Bryant SV, Gardiner DM. Regulation of dermal fibroblast dedifferentiation and redifferentiation during wound healing and limb regeneration in the Axolotl. Dev Growth Differ 2008, 50:743-754. 10.1111/j.1440-169X.2008.01072.x, 19046162.
6. Salley-Guydon JD, Tassava RA. Timing the commitment to a wound-healing response of denervated limb stumps in the adult newt, Notophthalmus viridescens. Wound Repair Regen 2006, 14:479-483. 10.1111/j.1743-6109.2006.00154.x, 16939577.
7. Bryant SV, Endo T, Gardiner DM. Vertebrate limb regeneration and the origin of limb stem cells. Int J Dev Biol 2002, 46:887-896.
8. Gardiner DM, Endo T, Bryant SV. The molecular basis of amphibian limb regeneration: integrating the old with the new. Semin Cell Dev Biol 2002, 13:345-352. 10.1016/S1084952102000903, 12324216.
9. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, Hanski I, Marden JH. Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 2008, 17:1636-1647. 10.1111/j.1365-294X.2008.03666.x, 18266620.
10. Parchman TL, Geist KS, Grahnen JA, Benkman CW, Buerkle CA. Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 2010, 11:180. 10.1186/1471-2164-11-180, 2851599, 20233449.
11. Animal Genome Size Database [http://www.genomesize.com], Animal Genome Size Database.
12. Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M, et al. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 2003, 302:842-846. 10.1126/science.1088305, 14593172.
13. Habermann B, Bebin AG, Herklotz S, Volkmer M, Eckelt K, Pehlke K, Epperlein HH, Schackert HK, Wiebe G, Tanaka EM. An Ambystoma mexicanum EST sequencing project: analysis of 17,352 expressed sequence tags from embryonic and regenerating blastema cDNA libraries. Genome Biol 2004, 5:R67. 10.1186/gb-2004-5-9-r67, 522874, 15345051.
14. Monaghan JR, Epp LG, Putta S, Page RB, Walker JA, Beachy CK, Zhu W, Pao GM, Verma IM, Hunter T, et al. Microarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration. BMC Biol 2009, 7:1. 10.1186/1741-7007-7-1, 2630914, 19144100.
15. Huggins P, Johnson CK, Schoergendorfer A, Putta S, Bathke AC, Stromberg AJ, Voss SR. Identification of differentially expressed thyroid hormone responsive genes from the brain of the Mexican Axolotl (Ambystoma mexicanum). Comp Biochem Physiol C Toxicol Pharmacol 2012, 155:128-135. 10.1016/j.cbpc.2011.03.006, 3166550, 21457787.
16. SGP/Sal-Site [http://www.ambystoma.org], SGP/Sal-Site.
17. Monaghan JR, Athippozhy A, Seifert AW, Putta S, Stromberg AJ, Maden M, Gardiner DM, Voss SR. Gene expression patterns specific to the regenerating limb of the Mexican axolotl. Biol Open 2012, 1:937-948. 10.1242/bio.20121594, 3507169, 23213371.
18. Campbell LJ, Suarez-Castillo EC, Ortiz-Zuazaga H, Knapp D, Tanaka EM, Crews CM. Gene expression profile of the regeneration epithelium during axolotl limb regeneration. Dev Dyn 2011, 240:1826-1840. 10.1002/dvdy.22669, 3297817, 21648017.
19. Holt RA, Jones SJ. The new paradigm of flow cell sequencing. Genome Res 2008, 18:839-846. 10.1101/gr.073262.107, 18519653.
20. Shendure J, Ji H. Next-generation DNA sequencing. Nat Biotechnol 2008, 26:1135-1145. 10.1038/nbt1486, 18846087.
21. Mardis ER. Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 2008, 9:387-402. 10.1146/annurev.genom.9.081307.164359, 18576944.
22. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010, 20:265-272. 10.1101/gr.097261.109, 2813482, 20019144.
23. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, et al. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST data sets. Bioinformatics 2003, 19:651-652. 10.1093/bioinformatics/btg034, 12651724.
24. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004, 32:D277-D280. 10.1093/nar/gkh063, 308797, 14681412.
25. Dungan KM, Wei TY, Nace JD, Poulin ML, Chiu IM, Lang JC, Tassava RA. Expression and biological effect of urodele fibroblast growth factor 1: relationship to limb regeneration. J Exp Zool 2002, 292:540-554. 10.1002/jez.10077, 12115937.
26. Poulin ML, Patrie KM, Botelho MJ, Tassava RA, Chiu IM. Heterogeneity in the expression of fibroblast growth factor receptors during limb regeneration in newts (Notophthalmus viridescens). Development 1993, 119:353-361.
27. Poulin ML, Chiu IM. Nucleotide sequences of two newt (Notophthalmus viridescens) fibroblast growth factor receptor-2 variants. Biochim Biophys Acta 1994, 1220:209-211. 10.1016/0167-4889(94)90137-6, 8312364.
28. Poulin ML, Chiu IM. Re-programming of expression of the KGFR and bek variants of fibroblast growth factor receptor 2 during limb regeneration in newts (Notophthalmus viridescens). Dev Dyn 1995, 202:378-387. 10.1002/aja.1002020407, 7626794.
29. Giampaoli S, Bucci S, Ragghianti M, Mancino G, Zhang F, Ferretti P. Expression of FGF2 in the limb blastema of two Salamandridae correlates with their regenerative capability. Proc Biol Sci 2003, 270:2197-2205. 10.1098/rspb.2003.2439, 1691501, 14613605.
30. Satoh A, Makanae A, Hirata A, Satou Y. Blastema induction in aneurogenic state and Prrx-1 regulation by MMPs and FGFs in Ambystoma mexicanum limb regeneration. Dev Biol 2011, 355:263-274. 10.1016/j.ydbio.2011.04.017, 21539833.
31. Gardiner DM, Blumberg B, Bryant SV. Expression of homeobox genes in limb regeneration. Prog Clin Biol Res 1993, 383A:31-40.
32. Gardiner DM, Blumberg B, Komine Y, Bryant SV. Regulation of HoxA expression in developing and regenerating axolotl limbs. Development 1995, 121:1731-1741.
33. Torok MA, Gardiner DM, Shubin NH, Bryant SV. Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol 1998, 200:225-233. 10.1006/dbio.1998.8956, 9705229.
34. Koshiba K, Kuroiwa A, Yamamoto H, Tamura K, Ide H. Expression of Msx genes in regenerating and developing limbs of axolotl. J Exp Zool 1998, 282:703-714. 10.1002/(SICI)1097-010X(19981215)282:6<703::AID-JEZ6>3.0.CO;2-P, 9846382.
35. Torok MA, Gardiner DM, Izpisua-Belmonte JC, Bryant SV. Sonic hedgehog (shh) expression in developing and regenerating axolotl limbs. J Exp Zool 1999, 284:197-206. 10.1002/(SICI)1097-010X(19990701)284:2<197::AID-JEZ9>3.0.CO;2-F, 10404648.
36. Carlson MR, Komine Y, Bryant SV, Gardiner DM. Expression of Hoxb13 and Hoxc10 in developing and regenerating Axolotl limbs and tails. Dev Biol 2001, 229:396-406. 10.1006/dbio.2000.0104, 11150241.
37. Tamura K, Yonei-Tamura S, Yano T, Yokoyama H, Ide H. The autopod: its formation during limb development. Dev Growth Differ 2008, 50:S177--187. Suppl 1.
38. Zakany J, Duboule D. The role of Hox genes during vertebrate limb development. CurrOpin Genet Dev 2007, 17:359-366.
39. Koniski A, Cohen N. Axolotl (Ambystoma mexicanum) lymphocytes produce and are growth-inhibited by transforming growth factor-beta. Dev Comp Immunol 1998, 22:91-102. 10.1016/S0145-305X(97)00044-X, 9617586.
40. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652. 10.1038/nbt.1883, 3571712, 21572440.
41. Robertson G, Schein J, Chiu R, Corbett R, Field M, Jackman SD, Mungall K, Lee S, Okada HM, Qian JQ, et al. De novo assembly and analysis of RNA-seq data. Nat Methods 2010, 7:909-912. 10.1038/nmeth.1517, 20935650.
42. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967. 10.1093/bioinformatics/btp336, 19497933.
43. Kumar A, Godwin JW, Gates PB, Garza-Garcia AA, Brockes JP. Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 2007, 318:772-777. 10.1126/science.1147710, 2696928, 17975060.
44. Miyazaki K, Uchiyama K, Imokawa Y, Yoshizato K. Cloning and characterization of cDNAs for matrix metalloproteinases of regenerating newt limbs. Proc Natl Acad Sci U S A 1996, 93:6819-6824. 10.1073/pnas.93.13.6819, 39111, 8692902.
45. Zeng L, Kempf H, Murtaugh LC, Sato ME, Lassar AB. Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somatic chondrogenesis. Genes Dev 2002, 16:1990-2005. 10.1101/gad.1008002, 186419, 12154128.
46. Schnapp E, Kragl M, Rubin L, Tanaka EM. Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 2005, 132:3243-3253. 10.1242/dev.01906, 15983402.
47. Kumar A, Velloso CP, Imokawa Y, Brockes JP. The regenerative plasticity of isolated urodele myofibers and its dependence on MSX1. PLoS Biol 2004, 2:E218. 10.1371/journal.pbio.0020218, 509293, 15314647.
48. Robert B, Sassoon D, Jacq B, Gehring W, Buckingham M. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J 1989, 8:91-100. 400776, 2565810.
49. Song K, Wang Y, Sassoon D. Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 1992, 360:477-481. 10.1038/360477a0, 1360150.
50. Muragaki Y, Mundlos S, Upton J, Olsen BR. Altered growth and branching patterns in synpolydactyly caused by mutations in HOXD13. Science 1996, 272:548-551. 10.1126/science.272.5261.548, 8614804.
51. McHedlishvili L, Epperlein HH, Telzerow A, Tanaka EM. A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors. Development 2007, 134:2083-2093. 10.1242/dev.02852, 17507409.
52. Laufer E, Nelson CE, Johnson RL, Morgan BA, Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 1994, 79:993-1003. 10.1016/0092-8674(94)90030-2, 8001146.
53. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.